Abstract

Our ideas about the intrinsically pathological nature of hallucinations and
delusions are being challenged by findings from epidemiology, neuroimaging and
clinical research. Population-based studies using both self-report and
interview surveys show that the prevalence of psychotic symptoms is far
greater than had been previously considered, prompting us to re-evaluate these
psychotic symptoms and their meaning in an evolutionary context. This
non-clinical phenotype may hold the key to understanding the persistence of
psychosis in the population. From a neuroscientific point of view, detailed
investigation of the non-clinical psychosis phenotype should provide novel
leads for research into the aetiology, nosology and treatment of
psychosis.

Psychosis is the price we pay for being what we are. And how unfair, how
bitterly unfair it is that the price is not shared around but paid by one man
in a hundred for the other ninety-nine.(Sebastian Faulks, Human
Traces)1

Hallucinatory experiences are as old as humankind and until the nineteenth
century these experiences were generally attributed to mystical or divine
sources such as gods or demons, whereas in modern times, hallucinations have
generally been regarded as pathological and as signs of
illness.2 Recently,
however, our ideas about hallucinations and delusions are being challenged by
findings from epidemiology. A new viewpoint is emerging. Simply put,
hallucinations and delusions are more common than we think. Population-based
studies using both self-report and interview surveys show that the prevalence
of psychotic symptoms is far greater than had been previously considered, with
a recent meta-analysis suggesting a prevalence rate of 5–8% in the
general population, which is about ten times higher than the prevalence of
diagnosed psychotic
disorders.3
Prevalence rates of such symptoms may be even higher among young people. Ten
years ago, Poulton et
al4 reported
that 14% of 11-year-old children in the Dunedin birth cohort reported
psychotic symptoms on interview and showed that these symptoms were associated
with a 5- to 16-fold increased rate of psychotic illness in early adulthood,
depending on the strength of the initial symptoms. Since then, large,
population-based studies surveying psychotic symptoms among adolescents have
found rates of 9–14% in interview-based
studies,5,6
and greater than 25% in some studies using self-report
questionnaires.7–9
Positive answers on self-report questionnaires have been validated on clinical
interview.9
Therefore it is becoming increasingly clear that a sizable minority of young
people experience psychotic symptoms.

This high prevalence of non-clinical psychotic symptoms in the population
prompts us to re-evaluate these symptoms in the light of evolutionary
theory.10 In this
editorial we discuss how this non-clinical phenotype (i.e. psychotic symptoms)
may hold the key to understanding the persistence of psychosis in the
population and provide a new perspective on aetiology and treatment.

Evolutionary theories of psychosis

Psychosis is highly heritable and exerts strong negative fitness effects.
Despite this apparent disadvantage, schizophrenia maintains a relatively
stable prevalence worldwide. Several theories drawing on the Darwinian
paradigm of selective advantage have been formulated to explain the
persistence of psychosis in the human population. Crow’s ‘
speciation’ hypothesis argues that psychosis is the ‘price
that Homo sapiens pays’ for development of
language.11 Burns
proposed that schizophrenia is a ‘costly by-product’ in the
evolution of complex social
cognition12 and
Nesse developed this idea further in terms of ‘cliff-edge’
fitness,13 whereby
certain traits may increase fitness up to a critical threshold, but beyond
this point, fitness falls precipitously. For instance, strong tendencies to
use metarepresentation and theory of mind can increase the ability to predict
other people’s behaviours and discern their intentions, but, as Nesse
explains, ‘it is only one step further, over the cliff’s edge of
psychotic cognition... to finding secret meanings and evidence for
conspiracies in other people’s most casual
gesture’.13
Recently, Dodgson & Gordon have proposed that certain types of
hallucinations could be viewed as evolutionary by-products of a cognitive
system designed to detect threat since, from a survival perspective, it is
much worse to fail to recognise a threat such as the sound of an approaching
predator than to mistakenly believe that a predator is approaching when it is
not.14 Evolution
may therefore favour a selective skew towards propagation of genes that
promote false positives over false negatives, thus resulting in ‘
hypervigilance hallucinations’ in the
population.14 In
social or pack animals, such as humans, hypervigilance is not necessary for
every member, but the presence of this trait in at least some members stands
to benefit the entire group. Such a trade-off allows the persistence of
advantageous traits even in the presence of increased risk of disorder.

Implications for genetic studies

The possibility that vulnerability to psychosis may be a by-product of ‘
normal’ human brain evolution, may offer an explanation for the
difficulty in locating a genetic ‘point of rarity’ between
individuals with schizophrenia and
controls.15,16
We would also suggest that the limited success in findings in schizophrenia to
date may be a result of shared genetic variation between the clinical
(disease) phenotype and the non-clinical (symptom) phenotype. Genetic research
thus far has used the simple dichotomy of people with psychotic disorder
compared with the general population. However, the relatively high prevalence
of the non-clinical psychosis phenotype in the general population may have
masked genes of importance. Rather than searching for genetic variation only
between individuals with psychotic disorders and the rest of the population
(which contains, as we have discussed, significant numbers of individuals with
the non-clinical phenotype), it may prove more fruitful to investigate genetic
variation among individuals with the non-clinical phenotype in the general
population (plus or minus individuals with the disease phenotype) compared
with the individuals without such symptoms. Furthermore, an understanding of
these genes and their functions may hold the key to explaining the persistence
of psychosis in the population. It is possible that there are evolutionary
advantages associated with genes that contribute to the non-clinical phenotype
but which, in a fitness trade-off, also increase the risk for psychotic
disorder. If, for example, as suggested by cliff-edge fitness
theory,10 psychosis
results from the development of certain useful traits beyond an optimal peak,
we might find that people with the non-clinical psychosis phenotype
demonstrate advantageous traits compared with the rest of the population in,
for example, certain language, cognitive or metacognitive skills. Detailed
investigation of the non-clinical psychosis phenotype might, therefore, allow
us to uncover a Darwinian explanation for the persistence of psychosis genes
in the general population that has not been possible by looking only at
psychotic disorder.

Implications for diagnosis and treatment

The current diagnostic nosological systems are undergoing revision.
Evolutionary theories lend support for the idea of a continuum approach to the
diagnosis of
psychosis15 and
provide some clues as to why the traditional Kraepelinian or categorical
approaches to psychosis are beginning to prove
problematic.16
Breaking down the categorical barriers may also help reduce the stigma
associated with psychosis, which remains one of the greatest obstacles
standing in the way of recovery and rehabilitation. Taking an evolutionary
perspective may also lead to changes in how we think about treatment –
for instance the idea of schizophrenia as a disorder of social brain
development points to the importance of family therapy and social skills
training. Some therapies such as hallucination-focused integrative therapy
already incorporate such elements alongside more traditional
cognitive–behavioural therapy
approaches.17 The
idea of hallucinations as a ‘hypervigilance’ reaction also
suggests the value of engaging directly with the content of the symptoms in
psychosis and acknowledging the fact that some individuals may wish to
preserve positive or ‘useful’ voices that they feel support or
help them.17

Broadening the evolutionary perspective

An evolutionary approach may also prove fruitful in other areas of
psychiatry. Higher than expected prevalences have been reported for depression
and anxiety. Prospective studies are showing that up to half (and perhaps even
a majority) of the population can expect one or more episodes of depression
over their
lifetime.18,19
Taking an evolutionary perspective, one could speculate that the tendency for
unhappiness and dissatisfaction is intrinsic to the human species (man as the ‘
unhappy ape’) and this is one of the features that has been a
contributory factor in the success of our species, driving Homo
sapiens onwards, even to the surface of the moon, in search of new
terrain and challenges. Applying evolutionary theories to depression may also
lead to new approaches to treatment and novel aetiological
theories.10

Conclusion

Charles Darwin’s anniversary year has ended but that does not mean we
should put the theory of evolution back on the shelf and dust it off only when
the next anniversary comes round. As Theodosius Dobzhansky famously stated, ‘
Nothing in biology makes sense except in the light of
evolution’.20
From a neuroscientific point of view, detailed investigation of the
non-clinical psychosis phenotype should provide novel leads for research into
the aetiology, nosology and treatment of psychosis and other mental
disorders.

Funding

M.C. is supported by a Health Research Board (Ireland)
Clinician Scientist Award and a NARSAD
Independent Investigator Award and is a member of the European
Network of National Schizophrenia Networks Studying Gene–Environment
Interactions (EU-GEI) funded by
EU–FP7.

Acknowledgments

We thank Alison Yung for suggesting the quotation from Human
Traces by Sebastian Faulks.